Orientation of the tetranuclear manganese cluster and tyrosine Z in the O2-evolving complex of photosystem II

An EPR study of the S2Y(z)· state in oriented acetate-inhibited photosystem II membranes

K. V. Lakshmi, Sandra S. Eaton, Gareth R. Eaton, Gary W Brudvig

Research output: Contribution to journalArticle

46 Citations (Scopus)

Abstract

Inhibitory treatment by acetate, followed by illumination and rapid freezing, is known to trap the S2Y(z)· state of the O2-evolving complex (OEC) in photosystem II (PS II). An EPR spectrum of this state exhibits broad split signals due to the interaction of the tyrosyl radical, Y(z)·, with the S = 1/2 S2 state of the Mn4 cluster. We present a novel approach to analyze S2Y(z)· spectra of one-dimensionally (1-D) oriented acetate- inhibited PS II membranes to determine the magnitude and relative orientation of the S2Y(z)· dipolar vector within the membrane. Although there exists a vast body of EPR data on isolated spins in oriented membrane sheets, the present study is the first of its kind on dipolar-coupled electron spin pairs in such systems. We demonstrate the feasibility of the technique and establish a rigorous treatment to account for the disorder present in partially oriented 1-D membrane preparations. We find that (i) the point-dipole distance between Y(z)· and the Mn4 cluster is 7.9 ± 0.2 Å, (ii) the angle between the interspin vector and the thylakoid membrane normal is 75°, (iii) the g(z)-axis of the Mn4 cluster is 70°away from the membrane normal and 35°away from the interspin vector, and (iv) the exchange interaction between the two spins is -275 x 10-4 cm-1, which is antiferromagnetic. Due to the sensitivity of EPR line shapes of oriented spin-coupled pairs to the interspin distance, the present study imposes a tighter constraint on the Y(z)-Mn4 point-dipole distance than obtained from randomly oriented samples. The geometric constraints obtained from the 1-D oriented sample are combined with published models of the structure of Mn- depleted PS II to propose a location of the Mn4 cluster. A structure in which Y(z) is hydrogen bonded to a manganese-bound hydroxide ligand is consistent with available data and favors maximal orbital overlap between the two redox center that would facilitate direct electron- and proton-transfer steps.

Original languageEnglish
Pages (from-to)12758-12767
Number of pages10
JournalBiochemistry
Volume38
Issue number39
DOIs
Publication statusPublished - Sep 28 1999

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Photosystem II Protein Complex
Manganese
Paramagnetic resonance
Tyrosine
Acetates
Membranes
Electrons
Thylakoids
Lighting
Proton transfer
Exchange interactions
Freezing
Oxidation-Reduction
Protons
Hydrogen
Ligands

ASJC Scopus subject areas

  • Biochemistry

Cite this

Orientation of the tetranuclear manganese cluster and tyrosine Z in the O2-evolving complex of photosystem II : An EPR study of the S2Y(z)· state in oriented acetate-inhibited photosystem II membranes. / Lakshmi, K. V.; Eaton, Sandra S.; Eaton, Gareth R.; Brudvig, Gary W.

In: Biochemistry, Vol. 38, No. 39, 28.09.1999, p. 12758-12767.

Research output: Contribution to journalArticle

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abstract = "Inhibitory treatment by acetate, followed by illumination and rapid freezing, is known to trap the S2Y(z)· state of the O2-evolving complex (OEC) in photosystem II (PS II). An EPR spectrum of this state exhibits broad split signals due to the interaction of the tyrosyl radical, Y(z)·, with the S = 1/2 S2 state of the Mn4 cluster. We present a novel approach to analyze S2Y(z)· spectra of one-dimensionally (1-D) oriented acetate- inhibited PS II membranes to determine the magnitude and relative orientation of the S2Y(z)· dipolar vector within the membrane. Although there exists a vast body of EPR data on isolated spins in oriented membrane sheets, the present study is the first of its kind on dipolar-coupled electron spin pairs in such systems. We demonstrate the feasibility of the technique and establish a rigorous treatment to account for the disorder present in partially oriented 1-D membrane preparations. We find that (i) the point-dipole distance between Y(z)· and the Mn4 cluster is 7.9 ± 0.2 {\AA}, (ii) the angle between the interspin vector and the thylakoid membrane normal is 75°, (iii) the g(z)-axis of the Mn4 cluster is 70°away from the membrane normal and 35°away from the interspin vector, and (iv) the exchange interaction between the two spins is -275 x 10-4 cm-1, which is antiferromagnetic. Due to the sensitivity of EPR line shapes of oriented spin-coupled pairs to the interspin distance, the present study imposes a tighter constraint on the Y(z)-Mn4 point-dipole distance than obtained from randomly oriented samples. The geometric constraints obtained from the 1-D oriented sample are combined with published models of the structure of Mn- depleted PS II to propose a location of the Mn4 cluster. A structure in which Y(z) is hydrogen bonded to a manganese-bound hydroxide ligand is consistent with available data and favors maximal orbital overlap between the two redox center that would facilitate direct electron- and proton-transfer steps.",
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T1 - Orientation of the tetranuclear manganese cluster and tyrosine Z in the O2-evolving complex of photosystem II

T2 - An EPR study of the S2Y(z)· state in oriented acetate-inhibited photosystem II membranes

AU - Lakshmi, K. V.

AU - Eaton, Sandra S.

AU - Eaton, Gareth R.

AU - Brudvig, Gary W

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N2 - Inhibitory treatment by acetate, followed by illumination and rapid freezing, is known to trap the S2Y(z)· state of the O2-evolving complex (OEC) in photosystem II (PS II). An EPR spectrum of this state exhibits broad split signals due to the interaction of the tyrosyl radical, Y(z)·, with the S = 1/2 S2 state of the Mn4 cluster. We present a novel approach to analyze S2Y(z)· spectra of one-dimensionally (1-D) oriented acetate- inhibited PS II membranes to determine the magnitude and relative orientation of the S2Y(z)· dipolar vector within the membrane. Although there exists a vast body of EPR data on isolated spins in oriented membrane sheets, the present study is the first of its kind on dipolar-coupled electron spin pairs in such systems. We demonstrate the feasibility of the technique and establish a rigorous treatment to account for the disorder present in partially oriented 1-D membrane preparations. We find that (i) the point-dipole distance between Y(z)· and the Mn4 cluster is 7.9 ± 0.2 Å, (ii) the angle between the interspin vector and the thylakoid membrane normal is 75°, (iii) the g(z)-axis of the Mn4 cluster is 70°away from the membrane normal and 35°away from the interspin vector, and (iv) the exchange interaction between the two spins is -275 x 10-4 cm-1, which is antiferromagnetic. Due to the sensitivity of EPR line shapes of oriented spin-coupled pairs to the interspin distance, the present study imposes a tighter constraint on the Y(z)-Mn4 point-dipole distance than obtained from randomly oriented samples. The geometric constraints obtained from the 1-D oriented sample are combined with published models of the structure of Mn- depleted PS II to propose a location of the Mn4 cluster. A structure in which Y(z) is hydrogen bonded to a manganese-bound hydroxide ligand is consistent with available data and favors maximal orbital overlap between the two redox center that would facilitate direct electron- and proton-transfer steps.

AB - Inhibitory treatment by acetate, followed by illumination and rapid freezing, is known to trap the S2Y(z)· state of the O2-evolving complex (OEC) in photosystem II (PS II). An EPR spectrum of this state exhibits broad split signals due to the interaction of the tyrosyl radical, Y(z)·, with the S = 1/2 S2 state of the Mn4 cluster. We present a novel approach to analyze S2Y(z)· spectra of one-dimensionally (1-D) oriented acetate- inhibited PS II membranes to determine the magnitude and relative orientation of the S2Y(z)· dipolar vector within the membrane. Although there exists a vast body of EPR data on isolated spins in oriented membrane sheets, the present study is the first of its kind on dipolar-coupled electron spin pairs in such systems. We demonstrate the feasibility of the technique and establish a rigorous treatment to account for the disorder present in partially oriented 1-D membrane preparations. We find that (i) the point-dipole distance between Y(z)· and the Mn4 cluster is 7.9 ± 0.2 Å, (ii) the angle between the interspin vector and the thylakoid membrane normal is 75°, (iii) the g(z)-axis of the Mn4 cluster is 70°away from the membrane normal and 35°away from the interspin vector, and (iv) the exchange interaction between the two spins is -275 x 10-4 cm-1, which is antiferromagnetic. Due to the sensitivity of EPR line shapes of oriented spin-coupled pairs to the interspin distance, the present study imposes a tighter constraint on the Y(z)-Mn4 point-dipole distance than obtained from randomly oriented samples. The geometric constraints obtained from the 1-D oriented sample are combined with published models of the structure of Mn- depleted PS II to propose a location of the Mn4 cluster. A structure in which Y(z) is hydrogen bonded to a manganese-bound hydroxide ligand is consistent with available data and favors maximal orbital overlap between the two redox center that would facilitate direct electron- and proton-transfer steps.

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